Going beyond personal protection against mosquito bites to eliminate malaria transmission: population suppression of malaria vectors that exploit both human and animal blood

Abstract

Protecting individuals and households against mosquito bites with long-lasting insecticidal nets (LLINs) or indoor residual spraying (IRS) can suppress entire populations of unusually efficient malaria vector species that predominantly feed indoors on humans. Mosquitoes which usually feed on animals are less reliant on human blood, so they are far less vulnerable to population suppression effects of such human-targeted insecticidal measures. Fortunately, the dozens of mosquito species which primarily feed on animals are also relatively inefficient vectors of malaria, so personal protection against mosquito bites may be sufficient to eliminate transmission. However, a handful of mosquito species are particularly problematic vectors of residual malaria transmission, because they feed readily on both humans and animals. These unusual vectors feed often enough on humans to be potent malaria vectors, but also often enough on animals to evade population control with LLINs, IRS or any other insecticidal personal protection measure targeted only to humans. Anopheles arabiensis and A. coluzzii in Africa, A. darlingi in South America and A. farauti in Oceania, as well as A. culicifacies species E, A. fluviatilis species S, A. lesteri and A. minimus in Asia, all feed readily on either humans or animals and collectively mediate residual malaria transmission across most of the tropics. Eliminating malaria transmission by vectors exhibiting such dual host preferences will require aggressive mosquito population abatement, rather than just personal protection of humans. Population suppression of even these particularly troublesome vectors is achievable with a variety of existing vector control technologies that remain underdeveloped or underexploited.

Figure 1

The proportions of blood meals obtained from humans by malaria vectors from the Americas, Asia, the Pacific and Africa. A recently published compilation of bionomic data for the world's most important vectors was filtered to exclude records representing undifferentiated mixtures of species from groups or complexes. In almost all cases, only records with estimates based on combined indoor and outdoor samples of mosquitoes were used. However, in the specific cases of Anopheles farauti and A. culicifacies species D, for which no data combining indoor and outdoor-caught samples were available, estimates based on outdoor-caught samples only were used. Also, for A. farauti, for which only one data point for sibling species-specific data was available from the contemporary data set, additional data was included from a historical study in which this species was identified morphologically in a setting where none of the other sibling species were present.

Figure 2

A schematic illustration of how malaria transmission intensity and responsiveness to personal protection varies according to vector preference for animals rather than humans. The simulations were implemented as previously described, except that the overall impact of personal protection measures (equivalent deterrent and insecticidal properties to a typical modern long-lasting insecticidal net assumed) are presented broken down by contributing underlying mechanism, and an Allee effect was incorporated. The entomological inoculation rate threshold below which elimination of malaria transmission may be feasible with existing diagnostic and therapeutic technologies (Orange horizontal line), was defined based on the most recent authoritative modelling studies.

Figure 3

The global distribution of malaria vector species known to feed readily on either humans or animals. Records of mosquito occurrence identified to the sibling species level using molecular methods were extracted from the Malaria Atlas Project database. The ranges for Anopheles darlingi, the A. fluviatilis complex, the A. culicifacies complex, A. lesteri and A. farauti complex were outlined using published data and expert opinions as previously described, while that for the Anopheles minimus complex was adjusted to incorporate newer records. The range for Anopheles arabiensis, previously defined using expert opinions, was updated to encompass newer records of this species. To generate an approximate range for Anopheles coluzzii (formerly A. gambiae M Form), the previous range for A. gambiae and A. coluzzii combined was adjusted to capture the areas where A. coluzzii has been recorded and exclude those where only nominate A. gambiae (formerly A. gambiae S Form) has been reported, using both data from the Malaria Atlas Project and an earlier map of the M and S forms of A. gambiae. The resulting data and ranges were overlaid on a map showing the limits of Plasmodium falciparum and P. vivax transmission.